Environmental Science and Pollution Research

, Volume 22, Issue 20, pp 15549–15562 | Cite as

Ectoine alleviates behavioural, physiological and biochemical changes in Daphnia magna subjected to formaldehyde

Research Article
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Accepted:

Abstract

Ectoine (ECT) is produced by halophilic microorganisms in response to various stressful factors. Its protective properties in bacteria and some populations of isolated cells are known; however, no data are available on its protective influence on aquatic invertebrates subjected to a common pollutant, formaldehyde (FA). The purpose of this study was to determine the effects of FA alone (at 20 and 60 mg/L) and in the combination with various concentrations of ECT (5, 10 and 25 mg/L) at various times of exposure on behavioural, physiological and biochemical parameters of Daphnia magna. Specifically, mortality, heart rate, thoracic limb movement, reduced glutathione (GSH)/oxidised glutathione (GSSG) ratio, catalase (CAT) activity and nitric oxide (NOx) levels were determined. The results showed that both concentrations of FA when administered alone induced significant alterations of the determined parameters. On the other hand, animals treated with the combinations of FA + ECT showed decreased mortalities, attenuated inhibition of heart rates and thoracic limb activities, less decreased GSH/GSSG ratios, lower stimulation of CAT activities and NOx levels when compared to the crustaceans subjected to FA alone. The most distinct attenuation of toxic effects was observed in the combinations in which the highest concentrations of ECT were used. The results suggest that oxidative stress induced by FA in daphnids is likely to be alleviated by the antioxidative action of ECT.

Keywords

Ectoine Formaldehyde Daphnia Glutathione Oxidative stress Catalase Nitric oxide 
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Notes

Acknowledgments

The authors wish to thank Promega Corp. for a free sample of GSH/GSSG assay kit and Prof. Tadeusz Skowroński for a word of advice.

References

  1. Abdel-Aziz H, Wadi W, Abdallah DM, Lentzen G, Khayyal MT (2013) Novel effects of ectoine, a bacteria-derived natural tetrahydropyrimidine, in experimental colitis. Phytomedicine: Int J Phytother Phytopharmacol 20:585–591CrossRefGoogle Scholar
  2. Adamian TI, Gevorkian ÉS, Voskanian AV, Minasian SM (2012) Antitoxic influence of taurine. Patol Fiziol Eksp Ter 2:39–41Google Scholar
  3. Ahmad I, Oliveira M, Pacheco M, Santos MA (2005) Anguilla L. oxidative stress biomarkers responses to copper exposure with or without beta-naphthoflavone pre-exposure. Chemosphere 61:267–275CrossRefGoogle Scholar
  4. American Society of Testing and Materials (1986) Standard practice for conducting static acute toxicity tests on wastewaters with daphnia: annual book of ASTM standards. ASTM: Phila 11.04:D4229–D4284Google Scholar
  5. Aruoma OI, Halliwell B, Hoey BM, Butler J (1988) The antioxidant action of taurine, hypotaurine and their metabolic precursors. Biochem J 256:251–255CrossRefGoogle Scholar
  6. Barata C, Varo I, Navarro JC, Arun S, Porte C (2005) Antioxidant enzyme activities and lipid peroxidation in the freshwater cladoceran Daphnia magna exposed to redox cycling compounds. Comp Biochem Physiol C Toxicol Pharmacol 140:175–186Google Scholar
  7. Bircan FS, Balabanli B, Turkozkan N, Ozan G (2011) Effects of taurine on nitric oxide and 3-nitrotyrosine levels in spleen during endotoxemia. Neurochem Res 36:1978–1983. doi: 10.1007/s11064-011-0521-3 CrossRefGoogle Scholar
  8. Boja JW, Nielsen JA, Foldvary E, Truitt EB (1985) Acute low level formaldehyde behavioural and neurochemical toxicity in the rat. Prog Neuro-Psychopharmacol Biol Psychiatry 9:671CrossRefGoogle Scholar
  9. Bownik A, Stępniewska Z (2015) Protective effects of ectoine on behavioral, physiological and biochemical parameters of daphnia magna subjected to hydrogen peroxide. Comp Biochem Physiol Part C: Toxicol Pharmacol 170:38–49Google Scholar
  10. Bownik A, Stępniewska Z, Skowroński T (2014) Protective effects of ectoine on heat-stressed daphnia magna. J Comp Physiol B 184:961–976CrossRefGoogle Scholar
  11. Bownik A, Stępniewska Z, Skowroński T (2015) Effects of ectoine on behavioural, physiological and biochemical parameters of daphnia magna. Comp Biochem Physiol Part C: Toxicol Pharmacol 168:2–10Google Scholar
  12. Casanova M, Morgan KT, Steinhagen WH, Everitt JI, Popp JA, Heck H’A (1991) Covalent binding of inhaled formaldehyde to DNA in the respiratory tract of rhesus monkeys: pharmacokinetics, rat-to-monkey interspecies scaling and extrapolation to man. Fundam Appl Toxicol 17:409–428CrossRefGoogle Scholar
  13. Fan WH, Cui MM, Shi ZW, Tan C, Yang XP (2012) Enhanced oxidative stress and physiological damage in daphnia magna by copper in the presence of nano-TiO2. J Nanomater 2012:7Google Scholar
  14. Finley JW, Wheeler EL, Witt SC (1981) Oxidation of glutathione by hydrogen peroxide and other oxidizing agents. J Agric Food Chem 29:404–407CrossRefGoogle Scholar
  15. Francis-Floyd R (1996) Use of formalin to control fish parasites. Cooperative Extension Servicek, University of Florida, 1–3Google Scholar
  16. Franklin P, Dingle P, Stick S (2000) Raised exhaled nitric oxide in healthy children is associated with domestic formaldehyde levels. Am J Respir Crit Care Med 161:1757–1759CrossRefGoogle Scholar
  17. Galinski EA, Pfeiffer HP, Truper HG (1985) 1, 4, 5, 6-tetrahydro-2-methyl-4-pyrimidinecarboxylic acid. A novel cyclic amino acid from halophilic phototrophic bacteria of the genus ectothiorhodospira. Eur J Biochem 149:135–139CrossRefGoogle Scholar
  18. Göller K, Galinski EA (1999) Protection of a model enzyme (lactate dehydrogenase) against heat, urea and freeze-thaw treatment by compatible solute additives. J Mol Catal B 7:37–45CrossRefGoogle Scholar
  19. Gómez-Oliván LM, Galar-Martínez M, Islas-Flores H, García-Medina S, SanJuan-Reyes N (2014) DNA damage and oxidative stress induced by acetylsalicylic acid in daphnia magna. Comp Biochem Physiol Part C: Toxicol Pharmacol 164:21–26Google Scholar
  20. Goth L (1991) A simple method for determination of serum catalase activity and revision of reference range. Clin Chim Acta 196:143–151CrossRefGoogle Scholar
  21. Graf R, Anzali S, Buenger J, Pfluecker F, Driller H (2008) The multifunctional role of ectoine as a natural cell protectant. Clin Dermatol 26:326–333CrossRefGoogle Scholar
  22. Griess P (1879) Bemerkungen zu der abhandlung der H.H. Weselsky und Benedikt ueber einige azoverbindungen. Chem Ber 12:426–428CrossRefGoogle Scholar
  23. Gurel A, Coskun O, Armutcu F, Kanter M, Ozen OA (2005) Vitamin E against oxidative damage caused by formaldehyde in frontal cortex and hippocampus: biochemical and histological studies. J Chem Neuroanat 29:173–178. doi: 10.1016/j.jchemneu.2005.01.001 CrossRefGoogle Scholar
  24. Hagar HH (2004) The protective effect of taurine against cyclosporine A-induced oxidative stress and hepatotoxicity in rats. Toxicol Lett 151:335–343CrossRefGoogle Scholar
  25. Harishchandra RK, Wulff S, Lentzen G, Neuhaus T, Galla HJ (2010) The effect of compatible solute ectoines on the structural organization of lipid monolayer and bilayer membranes. Biophys Chem 150:37–46CrossRefGoogle Scholar
  26. Janssen CR, Persoone G (1993) Rapid toxicity screening tests for aquatic biota. 1. Methodology and experiments with daphnia magna. Environ Toxicol Chem 12:711–717Google Scholar
  27. Kang KA, Lee KH, Chae S, Zhang R, Jung MS, Ham YM, Baik JS, Lee NH, Hyun JW (2006) Cytoprotective effect of phloroglucinol on oxidative stress induced cell damage via catalase activation. J Cell Biochem 97:609–620CrossRefGoogle Scholar
  28. Kim J, Kim S, An KW, Choi CY, Lee S, Choi K (2010b) Molecular cloning of daphnia magna catalase and its biomarker potential against oxidative stresses. Comp Biochem Physiol Part C: Toxicol Pharmacol 152:263–269Google Scholar
  29. Knapp S, Ladenstein R, Galinski EA (1999) Extrinsic protein stabilization by the naturally occuring osmolytes b-hydroxyectoine and betaine. Extremophiles 3:191–198CrossRefGoogle Scholar
  30. Koivisto S, Ketola M, Walls M (1992) Comparison of five cladoceran species in short- and long-term copper exposure. Hydrobiologia 248:125–136. doi: 10.1007/bf00006080 CrossRefGoogle Scholar
  31. Kriebel D, Myers D, Cheng M (2001) Short-term effects of formaldehyde on peak expiratory flow and irritant symptoms. Arch Environ Health 56:11CrossRefGoogle Scholar
  32. Lippert K, Galinski EA (1992) Enzyme stabilization by ectoine-type compatible solutes: protection against heating, freezing and drying. Appl Microbiol Biotechnol 37:61–65Google Scholar
  33. Lu Z, Li CM, Qiao Y, Yan Y, Yang X (2008) Effect of inhaled formaldehyde on learning and memory of mice. Indoor Air 18:77–83. doi: 10.1111/j.1600-0668.2008.00524.x CrossRefGoogle Scholar
  34. Lu C-L, Tang S, Meng Z-J, He Y-Y, Song L-Y, Liu Y-P, Ma N, Li X-Y, Guo S-C (2014) Taurine improves the spatial learning and memory ability impaired by sub-chronic manganese exposure. J Biomed Sci 21:51CrossRefGoogle Scholar
  35. Lyu K, Zhu X, Wang Q, Chen Y, Yang Z (2013) Copper/zinc superoxide dismutase from the cladoceran daphnia magna: molecular cloning and expression in response to different acute environmental stressors. Environ Sci Technol 47:8887–8893Google Scholar
  36. Ma TH, Harris MM (1988) Review of the genotoxicity of formaldehyde. Mutat Res 196:37–59CrossRefGoogle Scholar
  37. Malek FA, Möritz KU, Fanghänel J (2004) Effects of a single inhalative exposure to formaldehyde on the open field behavior of mice. Int J Hyg Environ Health 207:151–158CrossRefGoogle Scholar
  38. Martins J, Oliva Teles L, Vasconcelos V (2007) Assays with daphnia magna and Danio rerio as alert systems in aquatic toxicology. Environ Int 33:414–425CrossRefGoogle Scholar
  39. Metz B, Kersten GF, Baart GJ et al (2006) Identification of formaldehyde-induced modifications in proteins: reactions with insulin. Bioconjug Chem 17:815–822CrossRefGoogle Scholar
  40. Nagata S, Wang YB (2001) Accumulation of ectoine in the halotolerant brevibacterium sp. JCM6894. J Biosci Bioeng 91:288–293CrossRefGoogle Scholar
  41. Németh I, Boda D (1989) The ratio of oxidized/reduced glutathione as an index of oxidative stress in various experimental models of shock syndrome. Biomed Biochim Acta 48:53–57Google Scholar
  42. Ostadal P, Elmoselhi AB, Zdobnicka I, Lukas A, Elimban V, Dhalla NS (2004) Role of oxidative stress in ischemia-reperfusion-induced changes in Na+, K(+)-ATPase isoform expression in rat heart. Antioxid Redox Signal 6:914–923CrossRefGoogle Scholar
  43. Oudit GY, Trivieri MG, Khaper N, Husain T, Wilson GJ, Liu P, Sole MJ, Backx PH (2004) Taurine supplementation reduces oxidative stress and improves cardiovascular function in an iron-overload murine model. Circulation 109:1877–1885CrossRefGoogle Scholar
  44. Owen JB, Butterfield DA (2010) Measurement of oxidized/reduced glutathione ratio. Methods Mol Biol 648:269–277CrossRefGoogle Scholar
  45. Pastor JM, Bernal V, Salvador M, Argandoña M, Vargas C, Csonka L, Sevilla Á, Iborra JL, Nieto JJ, Cánovas M (2013) Role of central metabolism in the osmoadaptation of the halophilic bacterium chromohalobacter salexigens. J Biol Chem 288:17769–17781CrossRefGoogle Scholar
  46. Pflughoeft KJ, Kierek K, Watnick PI (2003) Role of ectoine in vibrio cholerae osmoadaptation. Appl Environ Microbiol 69:5919–5927CrossRefGoogle Scholar
  47. Pitten FA, Kramer A, Herrmann K, Bremer J, Koch S (2000) Formaldehyde neurotoxicity in animal experiments. Pathol Res Pract 196:193–198CrossRefGoogle Scholar
  48. Pushpakiran G, Mahalakshmi K, Anuradha CV (2004) Protective effects of taurine on glutathione and glutathione-dependent enzymes in ethanol-fed rats. Pharmazie 59:869–872Google Scholar
  49. Recio L, Sisk S, Pluta L, Bermudez E, Gross EA, Chen Z, Morgan KT, Walker C (1992) p53 mutations in formaldehyde-induced nasal squamous carcinoma in rats. Cancer Res 52:6113–6116Google Scholar
  50. Roessler M, Müller V (2001) Osmoadaptation in bacteria and archaea: common principles and differences. Environ Microbiol 3:743–754CrossRefGoogle Scholar
  51. Roychoudhury A, Haussinger D, Oesterhelt F (2012) Effect of the compatible solute ectoine on the stability of the membrane proteins. Protein Pept Lett 19:791–794CrossRefGoogle Scholar
  52. Sarkar S, Mukherjee S, Chattopadhyay A, Bhattacharya S (2014) Low dose of arsenic trioxide triggers oxidative stress in zebrafish brain: expression of antioxidant genes. Ecotoxicol Environ Saf 107:1–8CrossRefGoogle Scholar
  53. Schaffer S, Azuma J, Takahashi K, Mozaffari M (2003) Why is taurine cytoprotective? In: Lombardini B, Schaffer S, Azuma J (eds) Taurine 5. Kluwer Plenum, New York, pp 307–321CrossRefGoogle Scholar
  54. Shimizu N, Ogino C, Kawanishi T, Hayashi Y (2002) Fractal analysis of daphnia motion for acute toxicity bioassay. Inc Environ Toxicol 17:441–448CrossRefGoogle Scholar
  55. Sienkiewicz A, Vileno B, Pierzchała K, Czuba M, Marcoux P, Graczyk A, Fajer PG, Forró L (2007) Oxidative stress-mediated protein conformation changes: ESR study of spin-labelled staphylococcal nuclease. J Phys Condens Matter 19:285201CrossRefGoogle Scholar
  56. Smith KL, Galloway TS, Depledge MH (2000) Neuro-endocrine biomarkers of pollution-induced stress in marine invertebrates. Sci Total Environ 262:185–190CrossRefGoogle Scholar
  57. Swenberg JA, Gross EA, Randall HW Barrow CS (1983) The effect of formaldehyde exposure on cytotoxicity and cell proliferation. In: Clary JJ, Gibson JE, Waritz RS (eds) Formaldehyde toxicology, epidemiology, and mechanisms. Marcel Dekker, New York, pp 225–236Google Scholar
  58. Sydlik U, Gallitz I, Albrecht C, Abel J, Krutmann J, Unfried K (2009) The compatible solute ectoine protects against nanoparticle-induced neutrophilic lung inflammation. Am J Respir Crit Care Med 180:29–35. doi: 10.1164/rccm.200812-1911OC CrossRefGoogle Scholar
  59. Tang X-Q, Ren Y-K, Chen R-Q, Zhuang Y-Y, Fang H-R, Xu J-H, Wang C-Y, Hu B (2011) Formaldehyde induces neurotoxicity to PC12 cells involving inhibition of paraoxonase-1 expression and activity. Clin Exp Pharmacol Physiol 38:208–214CrossRefGoogle Scholar
  60. Tisler T, Zagorc-Koncan J (1997) Comparative assessment of toxicity of phenol, formaldehyde, and industrial wastewater to aquatic organisms. Water Air Soil Pollut 97:315–322Google Scholar
  61. Toews J, Rogalski JC, Clark TJ, Kast J (2008) Mass spectrometric identification of formaldehyde-induced peptide modifications under in vivo protein cross-linking conditions. Anal Chim Acta 618:168–183CrossRefGoogle Scholar
  62. Ton SS, Chang SH, Hsu LY, Wang MH, Wang KS (2012) Evaluation of acute toxicity and teratogenic effects of disinfectants by daphnia magna embryo assay. Environ Pollut 168:54–61CrossRefGoogle Scholar
  63. Ucmakli E, Armutcu F, Özturk A (2013) The effects of formaldehyde intoxication on the inducible nitric oxide synthase expression and nitric oxide level in the liver tissue of rats. Turk J Med Sci 43:52–56Google Scholar
  64. Unfried K, Kroker M, Autengruber A, Gotić M, Sydlik U (2014) The compatible solute ectoine reduces the exacerbating effect of environmental model particles on the immune response of the airways. J Allergy (Cairo). doi: 10.1155/2014/708458 Google Scholar
  65. USEPA (2002) Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms. U.S. Environmental protection agency office of water (4303T) 1200 Pennsylvania Avenue, NW Washington DC 20460, EPA-821-R-02-012Google Scholar
  66. van Dijken JP, Otto R, Harder W (1975) Oxidation of methanol, formaldehyde and formate by catalase purified from methanol-grown hansenula polymorpha. Arch Microbiol 106:221–226CrossRefGoogle Scholar
  67. Velki M, Stepić S, Hackenberger BK (2013) Effects of formalin on some biomarker activities of earthworms pre-exposed to temephos. Chemosphere 90:2690–2696CrossRefGoogle Scholar
  68. Vӧlker C, Boedicker C, Daubenthaler J, Oetken M, Oehlmann J (2013) Comparative toxicity assessment of nanosilver on three daphnia species in acute, chronic and multi-generation experiments. PLoS ONE 8(10), e75026. doi: 10.1371/journal.pone.0075026 CrossRefGoogle Scholar
  69. Wei YH, Yuan FW, Chen WC, Chen SY (2011) Production and characterization of ectoine by marinococcus sp. ECT1 isolated from a high-salinity environment. J Biosci Bioeng 111:336–342. doi: 10.1016/j.jbiosc.2010.11.009 CrossRefGoogle Scholar
  70. Welborn J, Manahan D (1995) Taurine metabolism in larvae of marine invertebrate molluscs (bilvalvia, gastropoda). J Exp Biol 198:1791–1799Google Scholar
  71. World Health Organization (2006) IARC Monographs on the evaluation of carcinogenic risks to humans: volume 88 formaldehyde, 2-Butoxyethanol and 1-tert-Butoxy-2-propanolGoogle Scholar
  72. Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol 208:2819–2830CrossRefGoogle Scholar
  73. Zhang L, Wang Y, Zhang C, Wang Y, Zhu D, Wang C, Nagata S (2006) Supplementation effect of ectoine on thermostability of phytase. J Biosci Bioeng 102:560–563CrossRefGoogle Scholar
  74. Zhang Z, Liu D, Bo Y, Liao Z, Tang L, Yin D, He M (2014) Taurine supplementation reduces oxidative stress and protects the liver in an iron-overload murine model. Mol Med Rep 10:2255–2262Google Scholar

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© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Department of Physiology and Ecotoxicology, Faculty of Biotechnology and Environmental SciencesThe John Paul II Catholic University of LublinLublinPoland
  2. 2.Department of Biochemistry and Environmental Chemistry, Faculty of Biotechnology and Environmental SciencesThe John Paul II Catholic University of LublinLublinPoland

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